Biosynthesis and Functions of Very-Long-Chain Fatty Acids in the Responses of Plants to Abiotic and Biotic Stresses

Abstract

Very-long-chain fatty acids (i.e., fatty acids with more than 18 carbon atoms; VLCFA) are important molecules that play crucial physiological and structural roles in plants. VLCFA are specifically present in several membrane lipids and essential for membrane homeostasis. Their specific accumulation in the sphingolipids of the plasma membrane outer leaflet is of primordial importance for its correct functioning in intercellular communication. VLCFA are found in phospholipids, notably in phosphatidylserine and phosphatidylethanolamine, where they could play a role in membrane domain organization and interleaflet coupling. In epidermal cells, VLCFA are precursors of the cuticular waxes of the plant cuticle, which are of primary importance for many interactions of the plant with its surrounding environment. VLCFA are also major components of the root suberin barrier, which has been shown to be fundamental for nutrient homeostasis and plant adaptation to adverse conditions. Finally, some plants store VLCFA in the triacylglycerols of their seeds so that they later play a pivotal role in seed germination. In this review, taking advantage of the many studies conducted using Arabidopsis thaliana as a model, we present our current knowledge on the biosynthesis and regulation of VLCFA in plants, and on the various functions that VLCFA and their derivatives play in the interactions of plants with their abiotic and biotic environment.

Keywords: Arabidopsis; elongation complex; sphingolipids; stress response; surface lipids; very-long-chain fatty acids.

Figure 1

Metabolic fates of very long-chain acyl-CoAs. VLC-acyl-CoA produced by fatty acid elongation complexes can be converted into aliphatic derivatives incorporated into the cuticle as cuticular waxes or serve as building blocks for the suberin biopolyester biosynthesis. VLC-acyl-CoA can be incorporated into storage lipids as triacylglycerols or in membrane lipids such as phospholipids (phosphatidylserine and phosphatidylethanolamine) or sphingolipids (ceramide, glucosylceramide and GIPCs). Abbreviations: CerS, ceramide synthase; FAH^ase, fatty acid hydroxylase; GCS, glucosylceramide synthase; GIPCs, glycosyl-inositolphosphoryl-ceramides; GT^ases, glycosyl-transferases; IPCS, inositolphosphoryl-ceramide synthase; IPUT, inositolphosphoryl-ceramide glucuronosyl-transferase; LCB DES^ase, LCB desaturase; VLC-acyl-CoA, very-long-chain-acyl-CoA.

Figure 2

Biosynthesis and selective involvement of VLC acyl-CoAs in the different lipid biosynthesis pathways in Arabidopsis. VLC acyl-CoAs are elongated from C16 and C18 long-chain fatty acids (LCFAs) synthesized in the plastid by the fatty acid synthase (FAS) complex. Plastidial saturated and monounsaturated C16 and C18 fatty acids are exported to the cytosol, where they are activated as acyl-CoAs by Long-Chain Acyl-CoA Synthetases (LACs). C16- and C18-CoA are then elongated into very-long-chain acyl-CoAs by the fatty acid elongation (FAE) complex. This complex consists of four enzymes localized in the reticulum endoplasmic membrane. Four sequential reactions lead to the addition of two carbon units: a condensation, a reduction, a dehydration and a final reduction, respectively, catalyzed by a β-Keto-acyl-CoA Synthase (KCS), a β-Keto-acyl-CoA Reductase (KCR), a 3-Hydroxyacyl-CoA Deshydratase (HCD) and an Enoyl-CoA Reductase (ECR). Different FAE complexes with different AtKCSs coexist in a same cell to produce VLC acyl-CoAs from C20 to C38. The resulting pool of acyl-CoAs is exploited towards the synthesis of different lipid categories such as membrane lipids (sphingolipids and phospholipids), surface lipids (cuticular waxes and suberin) and storage lipids (TAG). Abbreviations: ACP, acyl-carrier protein; CoA, Coenzyme A.

Figure 3

VLCFA content and distribution in Arabidopsis organs. (A) Distribution of long-chain (C16 and C18) fatty acids and VLCFA in Arabidopsis tissues (% of total); (B) VLCFA chain length distribution in Arabidopsis tissues (% of total); (C) Main lipid pools containing VLCFA in Arabidopsis tissues (% of total); Data for roots and stems were calculated from Delude et al. [60]. Note that for roots, the suberin polymer and soluble lipids were isolated and separately analyzed, while for stems waxes were first extracted, and waxes and dewaxed stem were separately quantified. For leaves and dried seeds global acyl-chain profiling, acyl-chain was released by transmethylation in 5% sulfuric acid in methanol for 3 h at 85 °C and silylated before GC analysis as for dewaxed stems in Delude et al. [59]. Unmodified C20 to C24 VLCFA were considered as phospho- or storage lipids, 2-hydroxy VLCFA as sphingolipids VLCFA, and typical waxes and suberin monomers as surface lipids VLCFA. For leaves and stems, the chain-length of the products from the decarbonylation pathway was considered as n + 1 (i.e., alkane C29 was counted in C30 VLCFA and derivatives).